Assessing the Effectiveness of Tuberculosis Management in Brushtail Possums (Trichosurus vulpecula), through Indirect Surveillance of Mycobacterium bovis Infection Using Released Sentinel Pigs.

In New Zealand, wild pigs acquire Mycobacterium bovis infection by scavenging tuberculous carrion, primarily carcasses of the main disease maintenance host, the brushtail possum (Trichosurus vulpecula). We investigated the utility of captive-reared, purpose-released pigs as sentinels for tuberculosis (TB) following lethal possum control and subsequent population recovery. Within 2-3 years of possum control by intensive poisoning, TB prevalence and the incidence rate of M. bovis infection in released sentinel pigs were lower than in an adjacent area where possums had not been poisoned. Unexpectedly, TB did not decline to near zero levels among pigs in the poisoned area, a fact which reflected an unanticipated rapid increase in the apparent abundance of possums. Monitoring infection levels among resident wild pigs confirmed that TB prevalence, while reduced due to possum control, persisted in the poisoned area at >20% among pigs born 2-3 years after poisoning, while remaining >60% among resident wild pigs in the nonpoisoned area. When fitted with radio-tracking devices, purpose-released pigs provided precise spatial TB surveillance information and facilitated effective killing of wild pigs when employed as "Judas" animals to help locate residents. Sentinel pigs offer value for monitoring disease trends in New Zealand, as TB levels in possums decline nationally due to large-scale possum control.

Comparison of ranging behaviour in a multi-species complex of free-ranging hosts of bovine tuberculosis in relation to their use as disease sentinels.

Sentinel species are increasingly used by disease managers to detect and monitor the prevalence of zoonotic diseases in wildlife populations. Characterizing home-range movements of sentinel hosts is thus important for developing improved disease surveillance methods, especially in systems where multiple host species co-exist. We studied ranging activity of major hosts of bovine tuberculosis (TB) in an upland habitat of New Zealand: we compared home-range coverage by ferrets (Mustela furo), wild deer (Cervus elaphus), feral pigs (Sus scrofa), brushtail possums (Trichosurus vulpecula) and free-ranging farmed cattle (Bos taurus). We also report in detail the proportional utilization of a seasonal (4-monthly) range area for the latter four species. Possums covered the smallest home range (<30 ha), ferrets covered ~100 ha, pigs ~4 km(2), deer and cattle both >30 km2. For any given weekly period, cattle, deer and pigs were shown to utilize 37­45% of their estimated 4-month range, while possums utilized 62% during any weekly period and 85% during any monthly period of their estimated 4-month range. We suggest that present means for estimating TB detection kernels, based on long-term range size estimates for possums and sentinel species, probably overstate the true local surveillance coverage per individual.

Reduced spillover transmission of Mycobacterium bovis to feral pigs (Sus scofa) following population control of brushtail possums (Trichosurus vulpecula).

In New Zealand, bovine tuberculosis (bTB) is present in domestic cattle and deer herds primarily as the result of on-going disease transmission from the primary wildlife host, the brushtail possum (Trichosurus vulpecula). However, bTB is also present in other introduced free-ranging mammalian species. Between 1996 and 2007, we conducted a series of studies to determine whether poison control of possum populations would have any effect on the prevalence of Mycobacterium bovis infection in sympatric feral pigs (Sus scrofa). We compared trends in the prevalence of bTB infection in feral pigs in six study areas: possum numbers were reduced in three areas, but not in the other three, effectively providing a thrice-replicated before-after-control-intervention design. Before possum control, the overall prevalence of culture-confirmed M. bovis infection in feral pigs was 16.7-94.4%, depending on area. Infection prevalence varied little between genders but did vary with age, increasing during the first 2-3 years of life but then declining in older pigs. In the areas in which possum control was applied, M. bovis prevalence in feral pigs fell to near zero within 2-3 years, provided control was applied successfully at the whole-landscape scale. In contrast, prevalence changed much less or not at all in the areas with no possum control. We conclude that feral pigs in New Zealand acquire M. bovis infection mainly by inter-species transmission from possums, but then rarely pass the disease on to other pigs and are end hosts. This is in contrast to the purported role of pigs as bTB maintenance hosts in other countries, and we suggest the difference in host status may reflect differences in the relative importance of the oral route of infection in different environments. Despite harbouring M. bovis infection for a number of years, pigs in New Zealand do not sustain bTB independently, but are good sentinels for disease prevalence in possum populations.

Longevity of Mycobacterium bovis in brushtail possum (Trichosurus vulpecula) carcasses, and contact rates between possums and carcasses.

AIM: To determine, for a variety of environmental conditions, how long Mycobacterium bovis might remain viable inside the carcass of a brushtail possum (Trichosurus vulpecula) that died of bovine tuberculosis (Tb), and to measure the rate of contact between free-ranging possums and possum carcasses. METHODS: Lesions of M. bovis were simulated by inoculating excised spleens weighing 0.5-1 g with 0.2 mL liquid culture containing approximately 5 x 10(7) cfu M. bovis/mL. Simulated lesions were inserted into possum carcasses (n=48) at the peripheral lymph nodes. Carcasses were placed in the field at two sites (a tussock grassland and a podocarp-broadleaved forest site) and in two seasons (summer and winter) for up to 62 days. Survival rates of M. bovis were estimated by sampling the simulated lesions over time, and culturing the recovered lesion to determine if any viable M. bovis bacteria were present. The time taken for a free-ranging possum to first encounter a dead possum in its home range was estimated by live-trapping possums and fitting them with proximity loggers (n=13). A 'contact' was recorded if these possums came within 40-50 cm of proximity loggers fitted to possum carcasses. RESULTS: There were strong seasonal and site effects in the survival rate of M. bovis in possum carcasses. In the grassland habitat, no viable bacilli were cultured from any carcass after 3 days in summer, whereas in winter all samples were culture-positive for the first 20 days, and some were still positive after 27 days. The survival rates for forest habitat were intermediate between the results for grassland, and there were no culture-positive carcasses after 9 days in summer or 27 days in winter. In summer, infected carcasses (n=6) were first encountered by possums a mean 1.9 (range 0.4-6.7) days after placement. CONCLUSIONS: Possum carcasses were contacted by free-ranging possums within the period that viable M. bovis were shown to survive in a carcass. The risk of such infection is likely to be most significant in winter or in areas with microhabitats where the survival of M. bovis is high. However, the generally low survival rate of M. bovis in possum carcasses and the low frequency of possum-to-carcass contacts indicate this route of transmission alone could not maintain Tb in a possum population.

Intraspecific transmission of Mycobacterium bovis among penned feral pigs in New Zealand.

We investigated intraspecific transmission of Mycobacterium bovis (etiologic agent of bovine tuberculosis [Tb]) among penned pigs (Sus scrofa) in New Zealand. Between 2002 and 2006, we conducted two trials, each involving two 1-ha pens in natural habitat in which uninfected sentinel pigs were kept with wild-caught feral pigs, many of which were infected with M. bovis. The rate of M. bovis transmission to sentinels was used to assess whether intraspecies transmission between live pigs could explain the high levels of infection in the wild population. In trial 1, no new infection was detected in 18 penned sentinels after total exposure of 3.9 yr (2.6 mo/sentinel); three of 11 sentinels in the wild became infected. In trial 2, a more heavily infected source pig population (94% prevalence compared with 42% in the first trial) was used, and one (4%) of 25 penned sentinels became infected. However, 75% of the eight sentinels released to the wild became infected. Combining trials, the difference in apparent annual incidence was significant (mean ± 95% confidence interval = 0.03 ± 0.12 for penned sentinels vs. 1.06 ± 6.74 for released sentinels; t=-3.51, P=0.04). In the pens, infected pigs were kept in contact with susceptible sentinels for 7 yr in total, but only one transmission event was detected. Taking pig longevity into account, the R(0) value (the basic reproductive rate of disease) for intraspecies infection between live pigs seems unlikely to exceed 0.25, even under highly conducive conditions. We suggest that live pigs are unlikely to transmit M. bovis to wild conspecifics often enough to sustain Tb in pigs by this route of transmission alone. The high prevalences seen in some New Zealand feral pig populations are likely to result from transmission from another host or route.